skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Cross-sexual Transfer Revisited
Abstract In her influential book “Developmental Plasticity and Evolution,” Mary Jane West-Eberhard introduced the concept of cross-sexual transfer, where traits expressed in one sex in an ancestral species become expressed in the other sex. Despite its potential ubiquity, we find that cross-sexual transfer has been under-studied and under-cited in the literature, with only a few experimental papers that have invoked the concept. Here, we aim to reintroduce cross-sexual transfer as a powerful framework for explaining sex variation and highlight its relevance in current studies on the evolution of sexual heteromorphism (different means or modes in trait values between the sexes). We discuss several exemplary studies of cross-sexual transfer that have been published in the past two decades, further building on West-Eberhard’s extensive review. We emphasize two scenarios as potential avenues of study, within-sex polymorphic and sex-role reversed species, and discuss the evolutionary and adaptive implications. Lastly, we propose future questions to expand our understanding of cross-sexual transfer, from nonhormonal mechanisms to the identification of broad taxonomic patterns. As evolutionary biologists increasingly recognize the nonbinary and often continuous nature of sexual heteromorphism, the cross-sexual framework has important utility for generating novel insights and perspectives on the evolution of sexual phenotypes across diverse taxa.  more » « less
Award ID(s):
2010841 2147567
PAR ID:
10468375
Author(s) / Creator(s):
;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Integrative And Comparative Biology
Volume:
63
Issue:
4
ISSN:
1540-7063
Format(s):
Medium: X Size: p. 936-945
Size(s):
p. 936-945
Sponsoring Org:
National Science Foundation
More Like this
  1. Mank, Judith (Ed.)
    Abstract Many animal species are haplodiploid: their fertilized eggs develop into diploid females and their unfertilized eggs develop into haploid males. The unique genetic features of haplodiploidy raise the prospect that these systems can be used to disentangle the population genetic consequences of haploid and diploid selection. To this end, sex-specific reproductive genes are of particular interest because, while they are shared within the same genome, they consistently experience selection in different ploidal environments. However, other features of these genes, including sex-specific expression and putative involvement in postcopulatory sexual selection, are potentially confounding factors because they may also impact the efficacy of selection asymmetrically between the sexes. Thus, to properly interpret evolutionary genomic patterns, it is necessary to generate a null expectation for the relative amount of polymorphism and divergence we expect to observe among sex-specific genes in haplodiploid species, given differences in ploidal environment, sex-limited expression, and their potential role in sexual selection. Here, we derive the theoretical expectation for the rate of evolution of sex-specific genes in haplodiploid species, under the assumption that they experience the same selective environment as genes expressed in both sexes. We find that the null expectation is that reproductive genes evolve more rapidly than constitutively expressed genes in haplodiploid genomes. However, despite the aforementioned differences, the null expectation does not differ between male- and female-specific reproductive genes, when assuming additivity. Our theoretical results provide an important baseline expectation that should be used in molecular evolution studies comparing rates of evolution among classes of genes in haplodiploid species. 
    more » « less
  2. Abstract Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci. Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution. 
    more » « less
  3. null (Ed.)
    Abstract Understanding diversity has been a pursuit in evolutionary biology since its inception. A challenge arises when sexual selection has played a role in diversification. Questions of what constitutes a ‘species’, homoplasy vs. synapomorphy, and whether sexually selected traits show phylogenetic signal have hampered work on many systems. Peacock spiders are famous for sexually selected male courtship dances and peacock-like abdominal ornamentation. This lineage of jumping spiders currently includes over 90 species classified into two genera, Maratus and Saratus. Most Maratus species have been placed into groups based on secondary sexual characters, but evolutionary relationships remain unresolved. Here we assess relationships in peacock spiders using phylogenomic data (ultraconserved elements and RAD-sequencing). Analyses reveal that Maratus and the related genus Saitis are paraphyletic. Many, but not all, morphological groups within a ‘core Maratus’ clade are recovered as genetic clades but we find evidence for undocumented speciation. Based on original observations of male courtship, our comparative analyses suggest that courtship behaviour and peacock-like abdominal ornamentation have evolved sequentially, with some traits inherited from ancestors and others evolving repeatedly and independently from ‘simple’ forms. Our results have important implications for the taxonomy of these spiders, and provide a much-needed evolutionary framework for comparative studies of the evolution of sexual signal characters. 
    more » « less
  4. Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems. 
    more » « less
  5. Larracuente, Amanda (Ed.)
    Abstract Genomes of aphids (family Aphididae) show several unusual evolutionary patterns. In particular, within the XO sex determination system of aphids, the X chromosome exhibits a lower rate of interchromosomal rearrangements, fewer highly expressed genes, and faster evolution at nonsynonymous sites compared with the autosomes. In contrast, other hemipteran lineages have similar rates of interchromosomal rearrangement for autosomes and X chromosomes. One possible explanation for these differences is the aphid's life cycle of cyclical parthenogenesis, where multiple asexual generations alternate with 1 sexual generation. If true, we should see similar features in the genomes of Phylloxeridae, an outgroup of aphids which also undergoes cyclical parthenogenesis. To investigate this, we generated a chromosome-level assembly for the grape phylloxera, an agriculturally important species of Phylloxeridae, and identified its single X chromosome. We then performed synteny analysis using the phylloxerid genome and 30 high-quality genomes of aphids and other hemipteran species. Unexpectedly, we found that the phylloxera does not share aphids’ patterns of chromosome evolution. By estimating interchromosomal rearrangement rates on an absolute time scale, we found that rates are elevated for aphid autosomes compared with their X chromosomes, but this pattern does not extend to the phylloxera branch. Potentially, the conservation of X chromosome gene content is due to selection on XO males that appear in the sexual generation. We also examined gene duplication patterns across Hemiptera and uncovered horizontal gene transfer events contributing to phylloxera evolution. 
    more » « less